Morphogenesis of the Acrosomal Vesicle During Spermiogenesis in the House Gecko
Ptyodactylus hasselquisti (Squamata, Reptilia)
The present study aimed to describe the morphogenesis of the acrosomal vesicle during spermiogenesis in the lizard Ptyodactylus hasselquisti. Five adult male lizards were captured during the period of sexual activity (April and May, 2005) from old houses in the city of Riyadh (25° 10' N, 46° 50' E), Saudi Arabia. Ultrastructural examination revealed proliferation and hypertrophy of Golgi complex elements as the initial event in formation of the acrosomal vesicle. Numerous small vesicles were released from Golgi complex and then coalesced to form a large proacrosomal vesicle which later attached to the proximal surface of spermatid nucleus. A proximal concavity appeared in the spermatid nucleus to completely lodge the acrosomal vesicle, then the spermatid nucleus with the lodged vesicle were transported to be directly apposed to the spermatid plasmalemma. This was associated with the appearance of a single acrosomal granule at the vesicle base. Subsequently, the progressively pushed acrosomal vesicle was flattened on the proximal nuclear surface. Some acrosomal vesicle deformities were also illustrated. The successive morphogenetic stages of the acrosomal vesicle were discussed in comparison with that reported in the previous studies concerned with spermiogenesis in other reptile species.
Spermiogenesis is the process by which haploid spermatids (gametes produced
by meiotic division) are transformed into mature spermatozoa (Hiatt
and Gartener, 1997; Stevens and Lowe, 1997; Young
and Heath, 2002).
The data derived from the ultrastructural studies on reptile's spermiogenesis
have clarified some aspects of fertilization and egg activation (Teixeira
et al., 1999). These ultrastructural data are also among the contributors
of phylogenetic analysis (Jamieson et al., 1995,
1999; Teixeira et al., 1999).
Ultrastructure of spermiogenesis and spermatozoa of lizards was the target of
considerable number of studies (Clark, 1967; Furieri,
1970, 1974; Del Conte, 1976;
Landim and Hoffling, 1977; Butler
and Gabri, 1984; Courtens and Depeiges, 1985; Al-Hajj
et al., 1987; Dehlawi and Ismail, 1990,
1991; Dehlawi, 1992; Dehlawi
et al., 1993; Teixeira et al., 1999;
Ferreira and Dolder, 2002, 2003;
Al-Dokhi, 2004; Mubarak, 2004;
Vieira et al., 2004; Al-Dokhi,
Formation of the acrosomal vesicle is one of the essential morphological transformations
during the process of spermiogenesis (Landim and Hoffling,
1977; Butler and Gabri, 1984; Al-Hajj
et al., 1987; Mubarak, 2004; Al-Dokhi,
2006). However, detailed ultrastructural description of the acrosomal vesicle
development in the lizard species has not yet been reported. Therefore, the
present study has been intended to elucidate the morphogenesis of the acrosomal
vesicle during spermiogenesis in the lizard Ptyodactylus hasselquisti
(P. hasselquisti). The obtained data would be helpful with the other
morphological studies to form a base for phylogenesis of lizard species.
Attention has been paid to compare the obtained results with that reported in the previous studies which are concerned with spermiogenesis in other lizard species.
MATERIALS AND METHODS
Five adult males of the lizard P. hasselquisti were captured during the period of sexual activity (April and May 2005), from old houses in the city of Riyadh (25° 10' N, 46° 50' E), Saudi Arabia. The lizards were dissected and their testes were removed, diced into proper small pieces (1 mm cubes) and immediately fixed by immersion in 3% buffered glutaraldehyde (0.1 M sodium cacodylate buffer at pH 7.2) for 4 h at 4°C. The fixed tissue specimens were thoroughly washed in the same buffer and then post-fixed in 1% osmium tetroxide (OsO4) in 0.1 M sodium cacodylate buffer (pH 7.2) for 2 h. Tissue specimens were subsequently dehydrated in ascending grades of ethanol and transferred to epoxy resin (Epon/Araldite mixture) via propylene oxide. Thin sections (70-80 nm) were cut with a diamond knife on an ultramicrotome (Leica, UCT), double stained with uranyl acetate and lead citrate and examined under a transmission electron microscope (JEOL, JEM1011) operating at 80 KV.
The differentiating spermatids occupied the adluminal compartment of the seminiferous epithelium. At the early stage of spermiogenesis, spermatids of P. hasselquisti displayed prominent juxtanuclear Golgi complex which consisted of flattened cisternae and many associated varied sized vesicles (Fig. 1). The cytoplasm of these early spermatids also contained abundant smooth endoplasmic reticulum, but scarce rough endoplasmic reticulum represented by flattened cisternae studded by tiny ribosomal granules. Mitochondria, ovoid or elliptical with linear cristae, were distributed throughout the spermatid cytoplasm. The content of the spermatid rounded nucleus was mostly a homogenous fine granular chromatin (euchromatin), with the presence of small patches of dense chromatin (heterochromatin) that were restricted to the inner side of the nucleolemma. The early spermatids were still rounded in shape. The first morphological event in the differentiating spermatids was the hypertrophy of Golgi complex and proliferation of its elements as represented by increasing number and size of its cisternae and associated vesicles (Fig. 2). The active Golgi complex was in a close contact with the spermatid nucleus. The associated Golgi complex vesicles continued to increase in size and subsequently a large voluminous vesicle developed, most likely through coalescence of many smaller vesicles (microvesicles) (Fig. 3). The resultant macrovesicle represented a proacrosomal vesicle which contained a flocculent material of low electron density.
With progression of the differentiation process, the proacrosomal vesicle moved
to attach the spermatid nuclear membrane (Fig. 4), with the
formation of an electron dense material at the site of attachment. This electron
dense material probably represented the initial appearance of a subacrosomal
material between the proacrosomal vesicle and the nuclear membrane.
||Early spermatid showing prominent Golgi Complex (GC). Nuclear
chromatin (CH) is uniformly fine granular (euchromatin), except for small
chromatin clumps (heterochromatin) on the inner nuclear membrane. Scale
bar = 1 μm
||Early spermatid manifesting conspicuous proliferated Golgi
Complex (GC) which involves varied sized vesicles at a juxtanuclear location.
Scale bar = 1 μm
||Large voluminous vesicle (V) (macrovesicle) formed as a result
of coalescence of smaller Golgi complex vesicles (microvesicles). There
is an intercellular bridge (arrows) connecting the two spermatids (*). Scale
bar = 1 μm
||A macrovesicle (V) (proacrosomal vesicle), arised from Golgi
complex, attached to the spermatid nucleus (N). An electron dense material
(arrow) has been formed at the site of attachment. Golgi complex (arrowhead)
is still in a close contact with the spermatid nucleus. Scale bar = 1 μm
||The proacrosomal vesicle (V) has enlarged and exerted more
pressure on the spermatid nucleus (N) which manifests a slight concavity.
The vesicle (V) contains a flocculent material. Scale bar = 1 μm
The nuclear surface at the site of attachment to the proacrosomal vesicle was
relatively flattened. The proacrosomal vesicle was still in intimate contact
with the active Golgi complex. While it was attached to the spermatid nucleus,
the proacrosomal vesicle continued to enlarge and Golgi complex microvesicles
were discerned joining the proacrosomal vesicle membrane (Fig.
The previously flattened nuclear surface showed slight concavity to accommodate the enlarging proacrosomal vesicle.
At a later stage, the acrosomal vesicle became a large outstanding structure
occupying a significant proportion of the spermatid cytoplasm (Fig.
6) and contained more flocculent material as well as remnants of degraded
membranous structures. The proximal concavity of the spermatid nucleus was increased
obviously and the subacrosomal material became distinct. A large number of microvesicles
were in a close association with the attached acrosomal vesicle. With advancing
of spermatid differentiation, the nuclear concavity was noticeably increased
to the extent that the acrosomal vesicle was completely lodged into the spermatid
nucleus (Fig. 7) which was still regularly rounded.
||The proacrosomal vesicle (V) has more enlarged and the proximal
concavity of the spermatid nucleus (N) has increased. The dense material
(arrow), between the vesicle membrane and the spermatid outer nuclear membrane,
became more obvious. Scale bar = 1 μm
||The Acrosomal Vesicle (AV) has been completely lodged into
the proximal concavity of the spermatid nucleus (N). Golgi Complex (GC)
is in a close contact with the acrosomal vesicle. Scale bar = 1 μm
At that stage, Golgi complex was remarkably active as evidenced by the presence
of numerous released microvesicles. The acrosomal vesicle was progressively
expanded to approach the spermatid periphery (Fig. 8) and
subsequently it was pushed against the spermatid plasma membrane (Fig.
The higher magnifications revealed the direct apposition of the acrosomal vesicle membrane to spermatid plasmalemma, as well as the compression of the vesicle (Fig. 10). Scattered electron dense varied sized granules appeared within the flocculent material contained in the acrosomal vesicle. The subacrosomal material was discerned as linear dense small patches arranged between the vesicle membrane and the spermatid nuclear membrane.
Compression of the acrosomal vesicle against the spermatid plasma membrane
was progressed and the subsequently flattened vesicle was recognized covering
a larger area on the proximal spermatid nuclear surface (Fig.
||The Acrosomal Vesicle (AV) has expanded to approach the spermatid
plasma membrane (arrow). Scale bar = 1 μm
||The Acrosomal Vesicle (AV) membrane has become directly apposed
to the spermatid plasma membrane (arrow). Scale bar = 1 μm
||Higher magnification showing the direct apposition of the
Acrosomal Vesicle (AV) membrane to the spermatid plasma membrane (arrow).
The acrosomal vesicle is apparently compressed. The subacrosomal material
(arrowheads) became more distinct and appears as linear dense patches. Scale
bar = 1 μm
||The Acrosomal Vesicle (AV) has been more compressed against
the spermatid plasma membrane (arrow). The flattened vesicle covers larger
area on the proximal surface of the spermatid nucleus (N). The vesicle still
contains flocculent material. Scale bar = 1 μm
||The Acrosomal Vesicle (AV) has been markedly pushed against
the spermatid plasma membrane (arrows). A small acrosomal granule (arrowhead)
has appeared at the base of the acrosomal vesicle. Heterochromatin (HC)
is densely packed as linear patches on the inner nuclear membrane. Scale
bar = 1 μm
This morphological change coincided with the appearance of a small dense granule
(acrosomal granule) on the base of the acrosomal vesicle (Fig.
12). Flattening of the acrosomal vesicle was associated with evident increase
in the size of the acrosomal granule which was also gradually flattened (Fig.
13). The later stage spermatids disclosed more compression of the acrosomal
vesicle and relative elongation of the spermatid nucleus (Fig.
Some spermatids showed a prominent acrosomal granule at the base of a non-flattened
lodged acrosomal vesicle (Fig. 15). However, such vesicles
were not apposed to the plasma membrane and located free within spermatid cytoplasm.
A small number of the growing spermatids disclosed acrosomal vesicles at different
morphogenetic stages, for instance some had flattened acrosomal vesicles with
prominent acrosomal granule and others possessed less flattened vesicles with
absence of the acrosomal granule (Fig. 16). Generally, the
growing spermatids displayed similar stage of acrosomal vesicle development,
e.g., spermatids showing acrosomal vesicles that were strongly pushed against
the spermatid plasmalemma (Fig. 17).
||The acrosomal granule (arrow) has enlarged and appears as
a dense body. The shape of the acrosomal granule conforms with that of the
compressed Acrosomal Vesicle (AV). Heterochromatin (arrowheads) is still
condensed on the inner nuclear membrane. Scale bar = 1 μm
||The Acrosomal Vesicle (AV) has been highly attenuated over
the proximal nuclear surface. The acrosomal granule (arrowhead) has been
also flattened. Scale bar = 1 μm
||A rounded Acrosomal Vesicle (AV) containing prominent acrosomal
granule (arrow) resting on its base and has lodged completely in the proximal
nuclear concavity. There is no apposition between the acrosomal vesicle
and the spermatid plasma membrane (arrowhead). Scale bar = 1 μm
||Spermatids (*) showing pushing and apposition of their Acrosomal
Vesicle (AV) against the corresponding plasma membranes. The vesicle on
the left is more flattened and contains distinct acrosomal granule (arrowhead)
and that on the right is less flattened with absence of apparent acrosomal
granule. Scale bar = 2 μm
||A number of growing spermatids (*) showing Acrosomal Vesicles
(AV) at the same morphogenetic stage. The acrosomal vesicles are directly
apposed to the spermatids plasma membranes and flattened over the proximal
nuclear surfaces. Scale bar = 1 μm
||A crescent-shaped Acrosomal Vesicle (AV) in a close contact
with Golgi complex (arrow) within a growing spermatid. Scale bar = 1 μm
||A poorly defined Acrosomal Vesicle (AV) with no distinction
between its membrane and the spermatid plasma membrane (arrow). Scale bar
= 1 μm
Relatively few spermatids displayed acrosomal vesicle deformities such as
crescent-shaped vesicles and the poorly-defined ones (Fig. 18,
The present study describes the developmental morphology of the acrosomal vesicle
in the lizard P. hasselquisti. The currently described acrosomal vesicle
morphogenesis is in accordance with the general events of sperm head differentiation
reported in other lizard species (Landim and Hoffling, 1977;
Butler and Gabri, 1984; Courtens
and Depeiges, 1985; Al-Hajj et al., 1987;
Mubarak, 2004; Al-Dokhi, 2006).
Acrosomal vesicle has been reported as an initial feature of sperm head differentiation
in reptiles (Butler and Gabri, 1984; Courtens
and Depeiges, 1985; Dehlawi and Ismail, 1990, 1991;
The initial event during the currently described acrosomal vesicle morphogenesis
was the hypertrophy and proliferation of Golgi complex elements which are known
to be integrated in packaging and transporting of the synthesized intracellular
materials (Stevens and Lowe, 1997). In case of acrosomal
vesicle, the accumulated substances within the vesicle are of an enzymatic nature,
mainly hydrolytic enzymes (Young and Heath, 2002), since
the acrosomal vesicle, which is considered a giant lysosome, is the precursor
of the sperm acrosomal cap. The latter structure mainly acts during fertilization
to disaggregate corona radiate cells and dissolve the zona pellucida by mean
of its hydrolytic enzymes, principally hyaluronidase.
The noticed close association between the acrosomal vesicle and Golgi complex elements obviously points to the origin of the vesicle from Golgi complex. It was evident in the present morphogenetic process that the proacrosomal vesicle had been formed as a result of fusion of the smaller vesicles released from the trans face of Golgi (exit face). Golgi complex cisternae and the associated vesicles were in a continuous intimate contact with the resultant proacrosomal vesicle and the subsequent acrosomal one. This observation confirms that the development of pro- and acrosomal vesicles requires continuous supply of the substances released from Golgi complex. This seems to be essential to increase the vesicle size and also to accentuate the concentration of the vesicle contents.
Attachment of the proacrosomal vesicle to the spermatid nucleus coincided with the appearance of the proximal nuclear concavity, which was most probably developed as a result of the pressure exerted by the proacrosomal vesicle on the spermatid nucleus. According to the present observation, the spermatid nuclear concavity is crucial for lodgment of the acrosomal vesicle.
The present results demonstrated that the spermatid nucleus and the lodged
vesicle had been transported from the cell center toward the cell periphery
to appose the vesicle membrane to the spermatid plasmalemma. This intracellular
translocation process was probably mediated by the cytoskeletal system, especially
the microtubular component. Microtubules have the ability to attach to membranous
organelles (e.g., mitochondria, vesicles), providing a mean by which such organelles
can be moved about within the cytoplasm (Young and Heath,
2002). In other words, the microtubular system is concerned with the transportation
processes within the cell cytoplasm. The present results revealed that flattening
of the lodged acrosomal vesicle on the spermatid nuclear surface had taken place
while the vesicle was pushed against the spermatid plasmalemma. Flattening of
the acrosomal vesicle has been demonstrated as the initial event in shaping
of the acrosomal cap during spermiogenesis in the lizard species (Landim
and Hoffling, 1977; Butler and Gabri, 1984; Courtens
and Depeiges, 1985; Al-Hajj et al., 1987;
Mubarak, 2004; Al-Dokhi, 2006).
It has been noticed in the present study that changing of the electron density
of the acrosomal vesicle occurs after flattening of the vesicle. In mammalian
spermatids, the electron translucent acrosomal vesicle enlarges and then condenses
and its content is transformed to an electron dense material (Lin
and Jones, 2000). We suppose that the nuclear pressure on the acrosomal
vesicle shares greatly in changing the vesicle electron density through reducing
its size with subsequent appearance of the acrosomal granule.
Presently, the initial appearance of the acrosomal granule has been noticed
while the acrosomal vesicle was flattened on the spermatid nucleus. The appearance
of the acrosomal granule is most probably the end result of a continuous concentration
process of the vesicle flocculent material. It has been reported that acrosomal
granule represents the condensed hydrolytic enzymes previously dispersed in
the acrosomal vesicle (Hiatt and Gartener, 1997). Currently,
a single large acrosomal granule was observed at the base of the acrosomal vesicle.
Presence of such single granule is a common finding in reptiles (Clark,
1967; Furieri, 1974; Del Conte,
1976; Butler and Gabri, 1984). However, multiple
acrosomal granules have been recognized in some reptilian species such as Scincus
mitranus (Al-Dokhi, 1996) and Agama adramitana
(Dehlawi et al., 1992). The single acrosomal
granule gives rise to an acrosomal medulla of uniform density in the sperm head,
while the multiple granules after dissolution result in acrosomal medulla of
varied density. In accordance with the present data, many other reptiles develop
the acrosomal granule after lodgment of the acrosomal vesicle to spermatid nucleus
(Dehlawi et al., 1990; Al-Dokhi,
2006). However, the lizard Stenodactylus selvini contradicts this
finding since it manifests the acrosomal granule before the mentioned lodgment
(Dehlawi et al., 1991).
Similarly, autherian mammals develop the acrosomal granule within the early
acrosomal vesicle before its lodgment to the spermatid nucleus (Holstein
and Roosen-Runge, 1981; Ploen and Courtens, 1986).
According to the present observations, most of the differentiating spermatids
disclosed a similar morphogenetic phase. This finding indicates that the spermatids
differentiation proceeds simultaneously. The presently illustrated intercellular
bridges between the growing spermatids play a role in such phenomenon, since
the information (cellular communication) can be transmitted between the spermatids
via these bridges (Hiatt and Garetner, 1997). Similar
intercellular bridges were described in some other lizard species (Landim
and Hoffling, 1977; Al-Hajj et al., 1987;
Dehlawi et al., 1990; Dehlawi,
1992; Mubarak, 2004; Al-Dokhi,
The intercellular cytoplasmic bridges is a sequence of incomplete meiotic division
due to a modified cytokinesis (Weiss and Greep, 1977;
Fawcett, 1991). Finally, the spermatids are connected
together to form a syncytium and the spermatids communicate through the bridges
and thus their activities are synchronized (Hiatt and Gartner,
1997). Additionally, some ectoplasmic specialization such as dense plates
between Sertoli cells share to establish a synchronous differentiation of spermatids
(Junqueira and Carreiro, 1980).
The noticed electron dense material between the acrosomal vesicle membrane
and nuclear membrane, represents the subacrosomal material which latter develops
into the rod shaped structure, the perforatorium, characteristic for reptiles
(Del Conte, 1976; Lin and Jones,
The currently illustrated acrosomal vesicle deformities were possibly developed
as a result of motility of the spermatid cytoplasmic contents. The currently
described morphogenetic events are involved in the Golgi and cap phases of spermiogenesis
(Hiatt and Gartener, 1997) and considered essential morphological
transformations during acrosome development (Sprando and
Russel, 1988; Lin et al., 1997).
The present data undoubtedly contribute in establishing the basic knowledge necessary for the researches concerned with phylogenesis in reptilian species.
This study was supported by a grant from Research Center-College of Science, King Saud University, Project No. (Zoo/2008/65). We gratefully acknowledge this support.
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